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Research Article

Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae

Sawyer Buckminster Fuller, Andrew D. Straw, Martin Y. Peek, Richard M. Murray, and Michael H. Dickinson
PNAS first published March 17, 2014; https://doi.org/10.1073/pnas.1323529111
Sawyer Buckminster Fuller
aSchool of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138;
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  • For correspondence: minster@seas.harvard.edu
Andrew D. Straw
bInstitute for Molecular Pathology, 1030 Vienna, Austria;
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Martin Y. Peek
cHoward Hughes Medical Institute Janelia Farm Research Campus, Ashburn, VA 20147;
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Richard M. Murray
dDivision of Engineering and Applied Sciences, California Institute of Technology, Pasadena, CA 91125; and
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Michael H. Dickinson
eDepartment of Biology, University of Washington, Seattle, WA 98195
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  1. Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved February 20, 2014 (received for review December 18, 2013)

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Significance

Insects are widely appreciated for their aerial agility, but the organization of their control system is not well understood. In particular, it is not known how they rapidly integrate information from different sensory systems—such as their eyes and antennae—to regulate flight speed. Although vision may provide an estimate of the true groundspeed in the presence of wind, delays inherent in visual processing compromise the performance of the flight speed regulator and make the animal unstable. Mechanoreceptors on the antennae of flies cannot measure groundspeed directly, but can detect changes in airspeed more quickly. By integrating information from both senses, flies achieve stable regulation of flight speed that is robust to perturbations such as gusts of wind.

Abstract

Flies and other insects use vision to regulate their groundspeed in flight, enabling them to fly in varying wind conditions. Compared with mechanosensory modalities, however, vision requires a long processing delay (~100 ms) that might introduce instability if operated at high gain. Flies also sense air motion with their antennae, but how this is used in flight control is unknown. We manipulated the antennal function of fruit flies by ablating their aristae, forcing them to rely on vision alone to regulate groundspeed. Arista-ablated flies in flight exhibited significantly greater groundspeed variability than intact flies. We then subjected them to a series of controlled impulsive wind gusts delivered by an air piston and experimentally manipulated antennae and visual feedback. The results show that an antenna-mediated response alters wing motion to cause flies to accelerate in the same direction as the gust. This response opposes flying into a headwind, but flies regularly fly upwind. To resolve this discrepancy, we obtained a dynamic model of the fly’s velocity regulator by fitting parameters of candidate models to our experimental data. The model suggests that the groundspeed variability of arista-ablated flies is the result of unstable feedback oscillations caused by the delay and high gain of visual feedback. The antenna response drives active damping with a shorter delay (~20 ms) to stabilize this regulator, in exchange for increasing the effect of rapid wind disturbances. This provides insight into flies’ multimodal sensory feedback architecture and constitutes a previously unknown role for the antennae.

  • stability
  • sensory fusion
  • feedback delay
  • system identification
  • turbulence

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: minster{at}seas.harvard.edu.
  • Author contributions: S.B.F., A.D.S., R.M.M., and M.H.D. designed research; S.B.F. and M.Y.P. performed research; S.B.F. and A.D.S. contributed new reagents/analytic tools; S.B.F. analyzed data; and S.B.F. and M.H.D. wrote the paper.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1323529111/-/DCSupplemental.

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Flies stabilize flight by sensing wind
Sawyer Buckminster Fuller, Andrew D. Straw, Martin Y. Peek, Richard M. Murray, Michael H. Dickinson
Proceedings of the National Academy of Sciences Mar 2014, 201323529; DOI: 10.1073/pnas.1323529111

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Flies stabilize flight by sensing wind
Sawyer Buckminster Fuller, Andrew D. Straw, Martin Y. Peek, Richard M. Murray, Michael H. Dickinson
Proceedings of the National Academy of Sciences Mar 2014, 201323529; DOI: 10.1073/pnas.1323529111
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